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Gut, 1975, 16, 337-342
The predictive accuracy of the postvagotomy insulin
test': A new interpretation
R. G. FABER, R. C. G. RUSSELL, J. V. PARKIN, P. WHITFIELD, AND
M. HOBSLEY
From the Department of Surgical Studies, The Middlesex Hospital and Medical School, London
SUMMARY Insulin-stimulated gastric secretion alone, without reference to basal secretion, has been
examined in 45 male patients with duodenal ulcer in whom no gastric operation had been performed and in 124 patients following vagotomy for duodenal ulcer. Gastric juice was examined
in terms not only of conventional indices, observed volume, titratable acidity and acid output, but
also VG, the volume corrected for pyloric loss and duodenal reflux.
The range of secretion of the unoperated subjects was established in terms of peak and half- to
two-hour values for all indices. By reference to these ranges, secretion of postvagotomy subjects
could be divided into two groups: (a) those with secretion within the preoperative range, and (b)
those with secretion less than the lower limit of the preoperative range.
The best discrimination was given by VG; those within the preoperative range (peak VG in excess
of 140 ml/hour and VG half to two hours in excess of 105 ml/hour) had a 50% liability to recurrent
ulcer, while those below the preoperative range had a zero liability to recurrent ulcer.
Of the conventional indices acid output gave the best discrimination, which was almost as good as
VG. Peak acid output of 8 mmol/hour or acid output one half to two hours of 5 25 mmol/hour
discriminated into two groups, with a 50% or zero liability to recurrent ulcer. Titratable acidity
(Hollander's index of secretion), being highly susceptible to reflux, was not an adequate discriminant.
Surgical division of the vagus nerves as a treatment
for duodenal ulceration was reintroduced by Dragstedt and Owens in 1943. After reporting preliminary
results on canine stomach pouches (Hollander,
Jemerin, and Weinstein, 1942) Hollander (1946)
described the use of the insulin test for detecting the
presence of intact vagal fibres in patients following
vagotomy. Two years later (Hollander, 1948) he
modified his criteria and defined a positive test as
one in which the free acidity in response to insulininduced hypoglycaemia was more than 20 mmol/
litre in excess of basal acidity. However he remained
cautious with regard to these criteria saying, 'At no
time have we stated that the test can predict the
chances that the patient will be relieved of his ulcer
or its symptoms, or that they will not recur at some
future date'. After another two years' experience he
'Based
on a paper read to the British Society of Gastroenterology
on another read to the Surgical Research Society
March 1974, and
July 1974.
Received for publication 23 January 1975.
in
in
clearly stated, 'The insulin test cannot be used to
prognosticate clinical results of vagotomy' (Weinstein, Hollander, Lauber, and Colp, 1950).
Many authors have suggested other criteria for
defining a positive test, culminating in the multiple
approach of Bank, Marks, and Louw (1967). They
used five criteria, those of Hollander (1948), Waddell
(1957), Bachrach (1962), Ross and Kay (1964), and
one of their own, and scored one plus for each
positive criterion. However, the value of any of the
newer criteria in predicting the likelihood of recurrent
ulceration in the individual patient rather than in
groups of patients was dismissed by Kronberg (1971)
who said: 'All these criteria have a higher discriminative ability than those of Hollander, but their
value in the diagnosis of recurrence is small.'
All criteria previously used have defined the result
of the insulin test in terms of a rise in secretion during
the insulin-stimulated period compared with the
basal period. Yet basal secretion is well known to be
very variable (Baron and Alexander-Williams, 1973).
It seemed to us, therefore, that insulin-stimulated
337
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338
R. G. Faber, R. C. G. Russell, J. V. Parkin, P. Whitfield, and M. Hobsley
secretion alone, without reference to basal secretion,
might with greater accuracy predict the liability to
recurrent peptic ulceration after vagotomy.
We have examined insulin-stimulated secretion not
only in terms of conventional indices, ie, observed
volume, titratable acidity, and acid output, but also
as VG, the observed volume of gastric juice after
correction for pyloric losses (Hobsley and Silen,
1969) and duodenal reflux (Hobsley, 1974).
Experimental Design and Patients
Each subject fasted and abstained from tobacco and
all medication known to affect gastric secretion from
midnight. From 9 am the subject lay semirecumbent
on a couch, a specially prepared two-lumen nasogastric tube (Thomson, Russell, and Hobsley, 1973)
was passed, and its correct position in the stomach
checked by the water recovery test of Hassan and
Hobsley (1970). In 123 subjects phenol red was,
throughout each study, instilled into the stomach via
the small lumen (Hobsley and Silen, 1969). After at
least a half-hour basal collection, soluble insulin
(0-2 units/kg) was injected intravenously, and gastric
juice was collected in 10-minute samples for a further
two hours. Venous blood samples, for the measurement of blood glucose, were taken at intervals
during the study, and only tests where adequate
hypoglycaemia (<40 mg/100 ml) (Sun and Shay,
1960) was obtained were included in this study.
Studies were performed on (1) 45 male patients
with duodenal ulceration, in whom no gastric
operation had been performed (unoperated subjects),
and in 37 of these patients phenol red was used; (2)
124 male patients following treatment for duodenal
ulcer by vagotomy (81 truncal, 35 selective, and eight
proximal gastric) with or without a drainage procedure, and phenol red was used in 86 of these
subjects. The length of follow up was between six
months and 10 years.
corrects for the presence of bile also. The correction
formula is:
Corrected reading = reading at 550 nm - 013511
(reading at 410 nm) + 0-0039.
The electrolyte estimations were checked by comparing the sum of the cations with the chloride
concentration (Hirschowitz, 1961). The phenol red
standard was handled as described by Hobsley and
Silen (1969).
The volume (Vobs) of each sample of gastric juice
was, in those cases where phenol red was used,
divided by the recovery fraction of phenol red to
determine the pyloric loss-corrected volume (Vcor).
The volume of duodenal reflux (VR) present in each
sample was calculated from the sodium output and
volume by the formula:
VR = 7-34 QNa - 0 0712 Vcor - 1-281
validated during insulin-stimulated secretion by
Faber, Russell, Royston, Whitfield, and Hobsley
(1974). This formula is an updated version of that
originally propounded by Hobsley (1974).
Results
UNOPERATED SUBJECTS
Gastric secretion corrected for pyloric loss and
duodenal reflux- VG
Gastric secretion was first examined in the 37
unoperated subjects in whom phenol red had been
used. The volume of secretion, expressed as VG ml/
hr, was determined for each of the four half-hour
periods following the injection of insulin (fig 1).
As the groups were not normally distributed, means
and standard errors were calculated after logarithmic transformation.
In the first half hour, secretion was always less than
in any of the subsequent half hours. The greatest
output was obtained sometimes in the second, sometimes in the fourth, but most often in the third half
hour, and the mean secretion during the third half
Methods and Calculations
hour was significantly greater than in the second
On each sample volume was determined, and, then (t = 3-78, p < 0-001) or fourth (t = 2-98, P < 0 01).
after filtration through Whatman's no 1 filter paper, In view of these findings, stimulated secretion was
the following measurements were made: titratable therefore expressed in two ways: (1) peak secretion,
acidity (Radiometer automatic titrator, titrations to defined as the sum of the VG of the three highest
pH 7), sodium, potassium, and chloride ion concen- consecutive 10-minute samples, multiplied by 2
trations (EEL flame photometer and chloride (ml/hr); (2) half- to two-hour secretion, which was
meter), and phenol red concentration (Unicam SP the sum of the VG of the nine samples during this
spectrophotometer at 550 and 410 nm). The reason period, divided by 1-5, thus again expressed as ml/hr.
for making readings at two wavelengths was to The ranges of secretion of the preoperative group, in
correct the phenol red readings for the presence of terms both of peak and half- to two-hour secretion,
blood and bile. The correction for blood was first were defined as being within two standard deviations
described by Crawford and Hobsley (1968), and of the mean (95 % tolerance limits) and are shown in
since then we have found that the same method figure 1.
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The predictive accuracy of the postvagotomy insulin test: A new interpretation
9
0
19
9
0
0
0
600_
339
I0
0
0
0
0
00
400_
0~~~
0
*0~~~~~~~~~
VG
ml/HOUR
S'1
200_
.~~~~~~~~~~~~~0
i
I1
1St
:o
324
-.
PEAK
4th
HOUR
HOUR
2HOUR RESPONSE 12-2 HOURS
2HOUR
Fig 1 Secretory response, VG ml/hour, to insulin 0-2 units/kg iv in 37 unoperated subjects:
(a) in each half hour after the injection of insulin; (b) peak value calculated as the sum of
the three highest consecutive 10-minute samples multiplied by 2 (ml/hour); (c) half- to twohour value as sum of secretion in second, third, and fourth half hours, divided by 1-5
(mi/hour). Means, standard errors of means, and 95 % tolerance limits have been
calculated after logarithmic transformation.
At the top is shown the numbers ofpatients whose secretion was greatest in the half hour
indicated. In some patients, peak secretion was greater than the value of the maximal
half hour, the three highest consecutive samples not being within one half-hour period.
CONVENTIONAL INDICES OF MEASUREMENT
Insulin-stimulated secretion was considered, in all
45 unoperated subjects, in terms of observed volume,
titratable acidity, and acid output. As with VG,
secretion during the first half hour was less than in
the subsequent three half-hour periods by all indices
of measurement. Therefore peak secretion and half- to
two-hour secretion were also calculated for these
indices and the preoperative ranges established. Like
VG, secretion expressed as observed volume or acid
output was distributed on a logarithmic scale, and
statistical analysis was performed after logarithmic
transformation. Unlike all the other indices of
measurement, it was found that the best way to
transform to a normal distribution the values of
secretion expressed as titratable acidity was to take
POSTVAGOTOMY SUBJECTS
Secretion corrected for pyloric losses and
duodenal reflux- VG
Stimulated secretion, expressed as VG ml/hr, in the
86 postvagotomy subjects in whom phenol red was
Observed Volume
Titratable Acidity
Acid Output
Va
(ml/hour)
(mmol/litre)
(mmol/hour)
(ml/hour)
Peak
Mean
Lower 95 % tolerance limit of range
Lower 99% tolerance limit of range
the square of each value. The 95% (ie, 2 standard
deviations from the mean) and 99% (ie, 3 standard
deviations from the mean) tolerance limits for each
group were calculated.
In table I, the mean values and lower 95 % and
99% limits of the range of each group are shown;
observed volume, titratable acidity, acid output, and
VG are all expressed as peak and half- to two-hour
secretion.
270
125
85
1-2 Hour
Peak
i-2 Hour
Peak
i-2 Hour
Peak
1-2 Hour
213
88
57
115
83
61
105
75
53
29-40
12-42
8-07
22-09
8-51
5 28
283
142
100
226
Table 1 Insulin-stimulated secretion in male patients with duodenal ulcer
105
71
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R. G. Faber, R. C. G. Russell, J. V. Parkin, P. Whitfield, and M. Hobsley
340
within the preoperative range. Likewise the secretion
in all four subjects with symptoms suggestive of
recurrent ulceration was within the preoperative
range. However, of the 73 subjects with no symptoms suggestive of recurrent ulceration, only six in
terms of peak secretion and seven in terms of half- to
two-hour secretion were within the preoperative
range; all other subjects secreted less than the preoperative group.
0
600
0
500-
A
as
400
Conventional indices of measurement
Insulin-stimulated secretion in all 124 postvagotomy
patients was compared with the preoperative range
ml/Hour
.Lt
of secretion, both peak and half-to two- hour values,
300in terms of observed volume (Vobs), titratable acidity,
and acid output.
In table II the distribution of patients relative to
vr0* v
200lower 95%Y. tolerance limit of the unoperated
the
Z
AW
group
is summarized. Only observed volume gave a
....A. .
discrimination of subjects into two groups to an
*
p1
extent comparable to that achieved in terms of VG.
c
100.
In terms of peak Vobs all patients with recurrent
ulcer or recurrent symptoms secreted within the preoperative range, and as Vobs half- to two-hours only
one patient with a recurrent ulcer secreted less than
the lower limit of this range. However, 16 and 20
PostPostPro-op
Pro-op
D.U.
D.U.
vagotomy
vagotomy
asymptomatic subjects were within the preoperative
ranges of the peak and half- to two-hour periods
I-2 HOUR RESPONSE
PEAK RESPONSE
respectively. Both titratable acidity and acid output
Fig 2 Comparison of secretion, expressed as VG, in
failed adequately to discriminate, because the number
the unoperated and postvagotomy groups. Mean,
of patients with recurrent ulcer below the lower
standard error of mean, and 95 % tolerance limits of
limits of the respective preoperative ranges was
range of the unoperated group calculated after
unacceptably high.
logarithmic transformation. In the postvagotomy group
In table III the distributions of patients in terms of
recurrent
with
closed circles represent patients
ulcer,
titratable
acidity and acid output relative to the
triangles patients with recurrent symptoms, and open
lower 99 % tolerance limits of the unoperated group
circles patients with no symptoms.
are summarized, and for comparison the Hollander
status is added. Titratable acidity one half to twoused compared with the preoperative range of hours still failed adequately to discriminate into two
secretion (95% tolerance limits) is shown in fig 2 groups, and, whereas peak titratable acidity did do
and summarized in table II. The VG of all nine so, 26 asymptomatic patients secreted within the prepatients who developed recurrent ulcers (eight seen operative range. Of the conventional indices, acid
at re-operation, one on gastroduodenoscopy) was output (fig 3) gave the b2st discrimination; when
VG
a
0
0
.
oh
0
0
0.
Observed Volume
Peak
Above Unoperated Lower 95 / Tolerance Limits
Recurrent ulcer .15
Recurrent symptoms .7
No symptoms .16
Below Unoperated Lower 95% Tolerance Limits
Recurrent ulcer
0
Recurrent symptoms .0
No symptoms .86
1-2 Hour
Titratable Acidity
Acid Output
VG
Peak
Peak
i-2 Hour
Peak
i-2 Hour
1-2 Hour
14
7
20
8
4
9
7
2
7
11
6
6
11
6
5
9
4
6
9
4
7
1
0
7
3
93
8
5
95
4
1
96
4
1
97
0
0
67
0
0
66
83
Table II Distribution o postvagotomy patients by reference to the unoperated lower 95 % tolerance limits
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The predictive accuracy of the postvagotomy insulin test; A new interpretation
Distribution by Our Criteria
Criterion
Distribution by Hollander Status
Clinical Status
Recurrent ulcer
Recurrent
symptoms
No symptoms
Recurrent ulcer
Recurrent
symptoms
No symptoms
Above
unoperated
lower 99 %
tolerance limits
Below
unoperated
lower 99 %
tolerance limits
341
Number in Terms of
Titratable Acidity
Number in Terms of
Acid Output
Peak
1-2 Hour
Peak
i-2 Hour
15
13
15
15
7
26
0
6
26
2
7
13
0
7
15
0
0
76
1
76
0
89
0
87
Criterion
Hollander
positive
Hollander
negative
Clinical Status
Number
Recurrent ulcer
Recurrent
13
symptoms
6
No symptoms
44
Recurrent ulcer 2
Recurrent
symptoms
1
No symptoms
58
Table III Distribution ofpostvagotomy patients by reference to two sets of criteria
compared with the lower 99 % tolerance limit of the
unoperated group all 15 patients with recurrent ulcer
and seven patients with recurrent symptoms were
above this value, together with only 13 and 15
asymptomatic subjects for the peak and half-to twohour periods respectively. As the numbers are not
identical, comparison between the discrimination in
terms of peak VG and peak acid output is difficult.
However, five of the 13 asymptomatic subjects
within the preoperative peak acid output range were
below the peak VG range.
By contrast, when examined by Hollander's
criteria two patients with recurrent ulcer and one
with recurrent symptoms were negative and 44
asymptomatic subjects were positive.
80
60
Acd
output
mEq/hout
i
40
A
Discussion
S
A
!'''
-----
'.'
A
20
0
Pr*-op
Post-
DLU.
vagotomy
Pr.ksponse
.
Poop
Post-
LL
vagoomy
f2Hour response
Fig 3 Comparison ofsecretion, expressed as acid
output, in unoperated and postvagotomy groups. Mean
and standard error of mean in the unoperated group
calculated after logarithmic transformation. The dotted
line represents the 95 % tolerance limits, and the lowest
closed line the lower 99 % tolerance limit of the
unoperated group. In the postvagotomy group closed
circles represent patients with recurrent ulcer, triangles
patients with recurrent symptoms, and open circles
patients with no symptoms.
Hollander's contribution (Hollander, 1946) was to
direct attention to insulin-induced hypoglycaemia as
a vagal stimulus to gastric secretion. However, his
fundamental approach to measurement of the
response to this stimulus was to compare gastric
secretion during insulin-induced hypoglycaemia with
the same subject's basal secretion immediately before
the insulin was given (Hollander, 1948). This was
merely an example of the technique of using the
subject as his own control, a technique of recognized
validity and proven worth in countless fields. Unfortunately, this approach depended on the assumption that basal gastric secretion is reproducible and
constant in any individual, and this assumption has
since been disproved (Baron, 1963; Gillespie, Elder,
Smith, Kennedy, Gillespie, Kay, and Campbell,
1972).
The present study has therefore ignored basal
secretion. As a standard for comparison, we have
replaced basal secretion after vagotomy with insulinstimulated secretion in male patients with duodenal
ulcer before vagotomy. We emphasize that our
findings, therefore, necessarily related only to male
Downloaded from http://gut.bmj.com/ on June 18, 2017 - Published by group.bmj.com
342
R. G. Faber, R. C. G. Russell, J. V. Parkin, P. Whitfield, and M. Hobsley
patients after vagotomy for duodenal ulcer. The
principle of our test is that the gastric secretion of
such patients during insulin-induced hypoglycaemia
is compared with the range of values obtained in a
group of patients with duodenal ulcer who had not
undergone vagotomy.
In making the comparison, we have studied not
only the conventional indices of gastric secretionvolume, titratable acidity, acid output-but also
VG, the volume of gastric juice after correction for
pyloric losses and duodenal reflux. In making the
comparison between data for unoperated patients
and data after operation we have used the 95 %
tolerance limits of the former for volume and VG
but the 99 % tolerance limits for titratable acidity and
acid output. These two indices are particularly liable
to negative errors occasioned by the reflux of
alkaline liquid from the duodenum into the stomach.
Because of this tendency we have found it necessary
to reduce the lower limit defining the unoperated
range in respect of these indices.
Our findings have been that volume, acid output,
and VG all give a much better prediction of recuffent
ulceration, proven or suspected, than the Hollander
criteria. The best prediction, as one might expect, is
given by the most accurate index of gastric secretion,
ie, VG: all patients with recurrence had an insulinstimulated secretion in the preoperative range, while
only six out of 73 patients with no evidence of
recurrence had a secretion level within that range.
Acid output and volume gave a reasonable, but
definitely less good, prediction; titratable acidity, the
basis of Hollander's criteria, gave a very poor
prediction. Since VG is the most accurate index and
its estimation requires the measurement of pyloric
losses, it was fortunate that the errors introduced by
bile into the spectrophotometric determination of
phenol red could be circumvented (see Methods).
The reason for the poor index given by titratable
acidity is presumably its great susceptibility to the
error produced by reflux of alkaline material from
the duodenum into the stomach; such reflux greatly
reduces titratable acidity both by dilution and by
neutralization. The mathematical relationships have
been fully explored by Fiddian-Green, Faber, Russell,
Whitfield, and Hobsley (1974). On the other hand,
reflux reduces acid output only by neutralization, and
the acid output therefore falls proportionately less
than does the titratable acidity. In retrospect, it was
unfortunate that Hollander chose not only basal
secretion as his standard for comparison, but
titratable acidity as his index of gastric secretionthe one index that is most susceptible to error.
The application of the criteria suggested in this
paper to past or future data on insulin-stimulated
secretion after vagotomy should, if there is any merit
in our approach, cast light on some other puzzling
features that have been reported: for example, the
apparent variability of the response to hypoglycaemia
at various times after the operation (Smith, Gillespie,
Elder, Gillespie, and Kay, 1972), and the disparity
in incidence of 'complete' and 'incomplete' vagotomy
from different centres.
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The predictive accuracy of the
postvagotomy insulin test: A new
interpretation.
R G Faber, R C Russell, J V Parkin, P Whitfield and M
Hobsley
Gut 1975 16: 337-342
doi: 10.1136/gut.16.5.337
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